ANt. S«. Enlomol. Fr. (N.S.). 1998. 34 (2): t49 • t62

COPULATORY MECHANISMS AND SEXUAL SELECTION IN THE LOPHOPIDAE

(HEMIPTERA : FULGOROMORPHA)

Adeline SOULIER-PERKINS & Thierry BOURGOIN l.abonio~ d'En~ 8t EP 90 d• CNRS. Mus<um N<ional d'Hlstoi:e -11c,

•s ruc Buffoa, 1<-1s oos Par!.

Resume. - Mkanismcs copulatolres et selection se.xuellt choz les Lophopidae (Htmiptera : Pulguromorpha). - L'6tudc morphologiquc compnrntivc de couples in copula de deux genres de Lophopidac (Hemiptera, Fulgoromorpha}. Jugoda Mclichnr et Pyri/la StAI, pennct d'aborder pour 1D premi~re fols duns ceue fomillc l'6tudc des mtcanismcs copu latoires mis c:n jcu. Pour l'cnsemble des Fulgoromorplu. soot mls en 6vidcna: le mlc imponalll quc pcut joocr le tube anal d3ns le mainticn de lo position copulatoirc e1 I• cli,·en;i16 des modes de uansport et de SIOCk.agc des spcmulOzoidcs. En ~Creoce i la 1li6orie de la s61Cdion scxuellc, cene divc:rsitE componcnltntalc et morphologiquc pournh s"interptttc:r commc compreoan1 autant d'ad.apiations au choix por les femelles el/ou l la comp6tition cntrc ml.les.. Un test de scbi.ario chcz. les Lophopidac, ponant sur lcs nlodificllions morphologiques du tube anal lcs rcconnai'i commc apomorphes, nc rcje1J1111 pas ainsi 111ypo~~ quc ces CIU'ICl~KS puissen1 constitucr au1an1 d'udApt11tlons pour ccs wa.

AbstrucL - The copulatory mcchnnisms are studied for the first lime within the Lophopidoe (Hemiplero, Fulgoromorpho) wilh !he cornp•muivc morphological study of !WO pairs preserved in c09ula : Jugoda Melichar and Pyrilla Sllll. As in 1hc whole Fulgoro1norphtt, it ahows the lmportant function or the anal tube to maintain the copulaiory position and 1he diversity for 1hc transport and storage of the spermatozoa. Morphological modificalion linltcd 10 the1e behaviours could be considered as :adapWions in the model of sexual selection where the males migb1 react to inlcr- or/and inlnSCJ<uol selective prcsswes. A 1eS1 of scenario recognlscs the morphological modifications of the anal tUbe u apomorphic char1c1ers: the hypoilte$is that Ihde characlus may rcprescnl adaptations for these wa cannot be n:jcctcd.

149

As with many groups of insects. male genitalia are widely used for taJ<.onomic purposes. In Hcmiptcra Fulgoromorpha, th.cy are usually complex enough 10 permil immediate recognition at a specific level. In return, the study of the female genitalia for the same 1uonomic pwposcs could be said 10 have been ocglectcd, lhe probable cause of this is due lo the fact they arc thought 10 be much more dclicotc, shrivel during preser,.atioo and subsequently. uruui111ble for in-depth srudy. However this prior Statemenl does nol bold true with the Fulgoromorpha (BOURGOIN. 1993 ; H UANG & BOURGOIN, 1993). Female genitalia seem 10 possess liulc useful infonnntion at the specific level (l'ENNAH, 1946). Several hypothesis in relation with sexual selection have tried 10 explain this complexity of male gcniml structures relatively 10 simpler female ones. Although intrascx ual selection is considered to be of primary importance in shaping male behaviours and morphologies associated with reproduction (Orr, 1994}, iotersexual 8Clcc1ion can also been advocated (EBERHARD, 1985, 1990}.

~1anl.ISC:rit acttplC k 23-1-1998.

150 A. SOULIER-PERKINS & T. BOUROOIN

Analysis of mating systems in planthoppers have been largely overlooked, only some very selected aspects are concerned and almost exclusively examined in the Delphacidae family (CLARIDGE & de VRUER, 1994; Orr, 1994). According to Orr (1994) no investigations have explicitly attempted to illustrate constraints acting on behaviour and morphology associated wilh reproduclion in this group. Such a statement is easily understandable because : I) morphology or male and female genital apparatus are far from lotally understood ; 2) data on copulatory mechanisms and mating behaviour are limited and 3) when available, data mainly result from 'horizontal analyses' (BOURGOIN, 1997), oflen non comparative, of ecological or behavioural studies which fail to recognise any reliable evolu1ionary significance to them because they lack the historical (= phylogenetical) background of 'vertical analyses' (GRt.NDCOLAS et al., 1997).

The mechanisms of copulation are even less known in Fulgoromorpba. very few studies have been undcnakcn, Uic first of which was done by WEBllR in 1930. Moreover, these srudies concern a very restric1ed sampling of the Fu.lgoromorpha diversity : only few genera have been srudied and other data are scattered in the litemrure (reviewed in SFORZA & BOURGOL'I, 1998)

This paper is lhe third of n series ( B OURGOIN & HUANG ; 1991 , SFORZn & BOURGOIN, 1998) dealing with copulatory mechanisms within the Fulgoromorpha. The purpose of this smdy is (i) 10 provide new data on male and female genitalia in a poorly investigated fwnily of Fulgoromorpha: the Lophopidac, (ii) lo describe for lhe first time the copula1ory mechanisms involved in two genera belonging to d ifferent major clades wilhln the Lophopidae. (iii) lo present a synthesis of what is currently known on the copulalory posilions and on the deposil and storage of spermatoia and (iv) 10 prescm a 1est of scenario implicating lhe shape of lhe male anal rubc in the Lophopidae. According to 1he sexual seleclion presented by EBERHARD (1985. 1990, 1991), I.be males should react to 1he female choice (inlersexual selective pressure) and /or to a compe1ition in between males (intrasexual selective pressure). The maintenance of the copulatory position and the spe.rm deposition linked to the shape of the male anal rube in the Fulgoromorpha allow us 10 1es1 1he hypolhcsis of the apomorpbic function of lhe elongaled hook-shaped or laterally and posteriorly developed male anal lube observed for some genera within the Lophopidae.

Material and methods

Dried preserved specimens of male and female geni1alia from 1wo differen1 genera of Lophopldae were ex.amincd: Jugoda Melk:hur. 191S, und l'yritla Su1J, l8S9. Copulatory bcll:i.viour was invcs1ig11tcd by dissection of dried pain preserved in copula ofJ11goda servufa Melichar. 191 S and Pyrilla prow/Jera11s S1Al, 1859.

Dissection nnd obscrvnLions were done acc.otding Lhc followlng protocol. 11•c: abdomens were remo­ved and placed lri a 10% KOH balh. wilh l-2drops ofblackchlo=.ol (CAAAYOll, J969)for ageneralendo· cuticular staining and raised to boiling fo1 5-10 nu1. Oro.."s dissection and cleaning of the abdomens were pcrfonncd in 70% alcohol. Finnl nnd precise dissections were done in diSlilled water with a Blue pmmgon staining and then 1ra.nsfcn:cd in glycerol for drawings using a camera luci.da Pairs preserved in copula were placed still joined In a cold t0% KOH balh for24h. After 12h bolh male and female abdomens were dissected. ncr()f(: final disseclion the spc:ciincn.s were stained in block chlora7.ol, directly in KOH.

For scanning electron microscopy CSEM), insects v.·ere dehydrated through increasing concentf'il· tions of alcohol, cri1ical point·dried, and co:ued wilh a 65-75 µm film of gold·polladium. They were exa· n1incd with A Jeol JSM 840 $Ct'lnning clcc::lron microscope.

Tenru used for 1he female genitalia are lhose of BoUROOIN (I 993) and for !he male geni1alio 1hose of BouROOIN (1988) and BOORoot• & HUAN<l (1990).

C0pufa1ory mn:harTIJ:nu and suual ,ftltctlon i11 tM Lophopldt1tt ISI

RESULTS

Female genitalia (figs 1-2)

Anal tube. In Jugoda, the :ma! rube, or segments X + XI. is large and flattened dorso­vcntrally (fig. I). Like a roor it covers Ilic gonoplocs. Jn Pyrilla, basely, the anal tube is nar­row (fig. 2). Its apical pact is l11rgely ex1cnded und disc-shaped in10 two amero-pos1criorly flanened lobes oriemcd ventrally.

·-fjg. I. fernalc genitalia or Jugoda scrn1ln ~fclichar, lateral Yicw. AT: anal tube ; AV : anterior vagina : HC :

butait copul.alrix : CO: conu11on oviduct : Gp/: gonoph1c : Lt: la~tetaitc IX : 0: goooporus; PV: pos1crior vaaina : SclP : 5C.krotini1.ed plate ; Sp : spcmuu.heca.

Segmenlal and apptndicular :rtru.cturei. In bodt genera, gonocoxae VID and ter­gum Vlil arc wenkly sclerolizcd. In Pyri/la the sacc.ulifonn structures are siill observable but reduced, while they are absent in Jugoda. Gonapophyses V1Il - first valvula of SNOl>­ORASS (1933) - are extremely l'Cduccd. La1ero1crgi1e IX are long and narrow and in the pro­longation to the 1crgu01 IX. Interiorly in Pyrilla, lalcrotergite lX and lergite IX are sepam­ted by a strong ln111.Sverse upodeme (fig. 2). absent in Jugoda. Gonapophyses IX or second valvul3C :uc present but reduced in Jugoda while they are reduced to a shon median mczn­branous lobe in Pyrilla. Goooplacs or third valvulae are two thick. more or less membnl­nous lobes, devoid of teeth and bearing SCIJIC. In Pyrilla the setac are patticularly developed on the dorsal margin or the dorsal lobe. Gonoplncs articulate postero-dorsally on the ful­crum. They are the only struc1ure of gonocoxal IX origin developed, in both genera, the gono­coxal plulc IX is ubsenL Anlero-ventrally to the loterotergite IX, the gonangulurn is otta­ched and appears as a small sclerotized plate. In Jugoda, the postc.rior vaginal process is present and orienled anirriody inside the general cavity but the gonospiculurn is absent as the gonospiculum bridge. 1bc gonospiculurn and the posterior vaginal process arc absent in Pyrilla.

Compl~x of the ectodermal geniJal ducts. TI1e complex of thc cclOdennal gcnilal duel is of monotrysian type. It opens exteriorly by the gonoporus, located between the gonopo­pbyses Vlll and D<. The two genera show a large bursa copulatrix opening directly into the vagina and covered with omamcniations on its U3 anterior. InJugoda three scleroli7.cd plates are observable in the vagina (fig. I) : a suoog plate is presem in the posterior wall of the posterior vagina, a second QOO is anached in the anterior wall or tlic posteri.or vagina and • third one is observable in the dorsal waU of the anterior vagina. The rwo first plates only nre presenl in Pyrilla and a pair of fuleral membranous pockets with thick walls are developed

152 A. SOUUER·PERKINS & T. BOURGOIN

on each side of the posterior vagina. The spennatbeca opens ventrally into the vagina and it is divided in101hrce distinct parts. lnlu8oda nn anterio.r 1ongue shaped pouch of the vagina is presenl between lhe spennatheca and the common oviduct ; this structure is much shor­ter in Pyri/la. The common oviduct opens into the venual wall of the anterior vagina. It is particularly large in Pyrr'lla.

Imm

•

Sp co

Fig .. ~ female genitalia or P)•rllfo pro111bera11s StAl. la1cnl view. AT: anal 1ube: BC : burs.a copula1rix: CO ; common oviduct : Gp! : gonopl!M: : /..I : latero·terg:ite IX ; Sp : spcnnlllhcca ; T VIII : tergite Vlll ; V: vagina.

Ttgumenuuy glands oft/1e bursa copulatrix (figs 34). Sclerotized ornamentations of the bursa copulalrix arc dislributed on two third anlcrior of the pouch. Jn both genera 1bey belong to the type 'pyrilla' (fig. 3) which is not circumscribed by a cuticular ring and which presen1s small in1emal crestS in the lumen of the bursa. A second type, more com­plex, is also present in the (.,ophopidae. This 1ypc, 'k:isscm1a type' (SouL1ER-l'ERK1Ns, 1997), shows an ornamentation limited by a circular cuticular ring,.bearing small cuticular digita­tions iu the lumen of the bursa (fig. 4).

Male genitalia (figs 5· 10)

The pygofer. The pygofer or 9tb abdominal segmen1 is present as a symmetric sclc· rotized ring excepted on its upper pan where it remains membranous. The posterior mem· braoe or diaphragm closes posteriorly the general cavi1y. It bears dorsally the anal tube (segments X and XJ) which is horizontally oriented in Jugoda (fig. 5) and strongly dcvclo· ped in an U-invened shape in Pyrilla (fig. 8). Two strong lateral apodemes are present on 1hc anterior la1eral margins of the pygofer.

The phallic compkx. The phallic complex is located between !he two gonostyli and protected dorsally by the anal tube. 'Three structures cau be recognized : the periandrium,

CtJplllatory mech1111Jsnu· and .fe:ruol stlection in lht LiJphDpidae 153

Figs 34, omc.mm1a1ion of lhc bur$a ce11>uh1ri~ culicufa.r wall obsen·cd on .sc1lf1ning clcclron microsc:opy. - 3, l)'pc 'Pyrilla', exlemal wall . -4, typc 'Kas:scroia', cx1ernal waU on the left and iotaoal \\'all oo the righl

the aedeagus and the endosoma. The periandrium is a structure more or Jess folded and complex, symmetrical, curved and dorsally concave. It is tube-like in Pyril/a (lig. 9) while in fttgoda (fig. 6) its half dorsal an1erior part is divided into two symmetrical wings to which apex is shaped as a spine externally oriented ; the second half of the periandrium is dorsally oriented and the apex is posieriorly jagged along its lenglh.

TI1e aedeagus is ulso a symmetrical structure. cliffed dorsally and ventrJlly and thus developed only laterally in pair formations. ht Jugoda, two tenrtinal processes of the aedea­gus are present and externally visible as they pass beyond the pcriandrium. The dorsal pro­cess(= prolongation of the aedeagus) points posteriorly, !he venual one(= aedeagal process s.s.) points antero-ventrally (fig. 7). ln Pyrilla the dom l process is absent (fig. 10). The ventral process beittS two spiniform formations which point respectively antero-ventrally and postero-<lorsally. Internally, the ductus seminis is short and opens veimaUy between the

154 A. SOULIER-PERKINS .t T. BOUROO!N

Intend partition of the ucdcagus. 11ie endosomn is always very reduced as in all the Lopho· piclae gt:nera.

AT

' DP 7 DP

VAP

En

Ed

Figs 5.7, male gcnitali1 or J~1tHlo 1tn•ula MtUchar. - 5, pygorcr and anal cube. - 6. phallic complex. -1. aedeagus L I. AT : anal lube ; DP : dorsal procas : DS : ducl1l> sc:minis : &I : oedeagus s. 1. ; En : endosoma ; Gn : a<>"""Yli ; P ; pcriandriwn : Py: pyaokr : V Al' ; ve'11tal anlerio< proccn

Tht gonDstyU. The gooos1yli arc a pair, symmetrical. well developed and scleroti· w:I. Their dorsal m1111ins arc irregularly s.hJlped. A spine-lilcc process is present externally and ventrally oriented. A strong dorso-basal rounded process is present in Jugoda. The apo­demcs arc well developed and arc equivalent IO 1/3 of the size of the gooostyli in Jugoda; they are less developed in Pyrilla. The lamina Fgonostyll is absent.

AT

' VPP

VAP

Go p

JO VPP

OS I •m VAP

Figs 8· 10, malt g.:ni1ali1 or l'yrilla prorub<t<lllJ SIU. - 8. pyio(cr Ind 111al wbe. - 9, pballic: comple<. - 10. -.,,.. s. I. AT : ona1 IUbc: CC : corpw conncctivl : DS : ductlU 1emini1 ; E.d : llC<k>&IU 1. L; En : ~; G• : ~Ii ; P: pcriaodriwn ; Py : pyc<>(cr. T: l<>Ctiduclus : Tes : leelirorm 11roau1< ; VAi': va11nl 1111crior process; VPP: vcnltal ~ p<oCQL

155

Copulatory mechanism

Jugoda S<f11ula Melichar, (figs 11- 12)

On city material, copulatory position is unnatural a.~ female and male arc head to foot, bodies end to end with the male abdomen fncing dorsaUy (fig. 11).

During mating the aedeagus and the periandrium are strongly eve.rted and both are inserted into the female vagina. Male gonostyl i come to settle deeply with !heir dorsal cxlcnsion into the intcrscgmcntal membranous area vn.vm. posteriorly to the seventh s1emite (fig. 11 ). The male anal tube is miscd and moved backwards to press the Vil abdo­minal segmcnl of the female (fig. 11). Both of 1hcsc mechanisms hold the female in posi­tion during mating. The diaphragm is visil>le lncerally. The phallic complex is inserted through the fernt\le gonoporus into the vagina where ii rests on the two venlI3! selerites of the female genital ducts (fig. 11 ). The postcro·vcn1ral vaginal sclerite would appear to have swung into the anterior pouch of the vagina between 1he spennatheca and the common ovi­duct.

TVIU Lt

Opj

v Ou

SclP co

PC

lam

PY

12

1l I """

ri&' 11 · 12, Ju1otla 1cn·11/<1 t-1clh:hat. - 11, male 11ul ftrr111le &t.lnllallh in cupulnlory pos,icion. AT ; nn.11 tube : CO: COlfuoon oviduct : Gp/: goooploc: Gn : gonoityli : /.I : la1U0-1ergi1e l.X : PC: phallic complex: Py: pyaorc:r: SclP : 1dcrocini1.cd phuc; Sp: spcrnuuhec1 : 1' VIII : 1ctgllc VJTI : V: wgin~

Pyrll/a prolubtrons St!IJ, 1859 (figs 13-14)

The same copulatory position is observable in Pyrllla (fig 13) andJ11goda. The mole gonos1yli enclose each of the female gonoplacs on their ventral external side. The anal lube is raised and moved backwards and its apex hooks the bac.I:. of the Vil abdominal segment or the fcmt\lc (fig. 13). The phallic complex (acdCAgus and periandrium) is inscncd into the vagina. The ventral pan of the phallic complex rests on 1he dorsal sclerite of the vagina and its apex is lodged on the an1ero-ventral sclcritc of lhc vagina (fig. 13).

156 A. SOUUER-PERXJllS I< T. BOllRGOL'I

T Vlll

I mtn

14 13

Fip 13-14, l'}n/la prot1•b<r""I SIAI. - ll • .We and lcmak acrul>li• in copulaU><y posilicn. ,._T : enal 1ubc ; BC : ~ ..,.,..wtu : CO : c:anmoo oviducl : GPf : gonoploc : Gn : g0ll05<}'li : /.J : lateto 1~1e IX : PC : pll>lb< complu ; f'y : pygo(cr ; S<I/' : Klcrotiruud pl>IC ; Sp : spcnnalhoca ; T VIII : ~IC VIII. - 14. schematic rtpresenwion of the male and female geni~lia in c:opulata.y position.

DISCUSSION

Morphology of male and female genitalia In Lophopidae. - Female geniialia of J11g0</a and Pyrilla rue good representatives of1he general female genitalia co11J'orn1ntion in Lophopidae (SOOLIER·PERKINS, 1997). In the Hemiptcra, lhey belong to the l:icini3n·shaped type (DUPUIS. I 9SS) in which gooapophysian structures mainly are modified while gono­coxal ones remain practically unchanged. Such type is gcncl'lll in Fulgoromorpha and wi1hin the Lopbopidae ii belongs to the fulgoroid l)'pC as proposed by BoURGOL~ (1993). The major characteristics or female geniutlia in this family are (fig. 2): I) the latero-venual modi· fication of the la1cro1ergi1c IX in a long and elongate pln1e; 2) lhc very reduced gonocoxae IX carrying slrongly developed gonoplacs: 3) the absence of the gooospiculum; 4) the great reduction of the gonupophysian siructures VU! and IX and S) 1be presence of anal lobes (SOii· LIER·PERKJNS, 1997).

In bolh gcncm the bursa copulall'ix opens widely into the an1erior vagina. The sclc­rotized ornamentations of the bursa copulatrix are probably impression of tegumentary glands. While lhcse glands arc present in many Fulgoromorphn tru<a (SFORZA & BOURGOIN, 1998) their role is still unclear and will have to be elucidated in the future (but sec below). 1be aruerior tongue shaped pouch of the anterior vagina observed inJugoda corresponds to a particular confonnaiion of !his part of lhe vagina also present in various olhcr Lophopi· daegenera.

The phallic sll'Uctures are often complex in Lophopidae and without dissection. it is impossible 10 dis1inguish between structures belonging to the periandrium or 10 the acdea­gus and pm1icularly bclween the periandrium processes and tl1e ones carried by 1hc acdcn­gus. This has lead to some odd imerpreialiOQS wi1h the presence of paired phalli in Lophops and £/asmoscells (CHAN & YANG, 1989).

As s1udied by SOULIER-PERKINS (1997), the male genitalia lopbopid type agrees withou1 any difficulty with the other fulgoromorph types studied by BOIJRGOL~ ( 1988) and BoURGOIN & liUAllG ( 1990).

Copulatory m~chanisnu: and saual 3elet:tion in 1he lophopidoe 157

Copulatory mechanism. - Very few infonnation is known concerning the copula· tory mechanisms in Fulgoromorpha. This even concerns few families on lhe 1wenty currently recognii.ed : the Cixiidae (WEBER, 1930; HOCH & REMANE, 1985; SFORZA & BOURGOIN, 1998), the Delphacidae (ASCHE, 1985; HEADY & WILSON, 1990). the lssidae (MYERS, 1928; WEBER. 1930) and 1he Tropiduchidae (BOURGOIN & HUANG, 1991 ). Some punctual iofor· mation for sperm depository into the female genitalia can also be found for other Fulgoro­morpha families in STROB!NO (1955) for Dic1yopharidae, in BOURGOIN & HUANG ( 1991) for Tenigomeuidae or in BOURGOIN (1993) for rhe Fulgoromorpha in general.

lf it is therefore roo early ro look if any general pauem emerges but, at least, two interesting points need 10 be analysed with more details: (I) the role of the male anal rube in the mainienancc of the copulatory position and (2) the mode of sperm deposition and sto­rage in the Fulgoromorpha.

Maintenance of lhe copulatory position. - Live specimens have not been observed in a copulatory position. TI1e specimens studied and described herewere dry and preserved in copula which is the case for most observed Fulgorornorpha (MYERS, 1928 ; HUANG & BOllRGOIN. 1993} and subsequen1ly, 1he general position of the male with the respect to that of the female is probably unatural. As observed by HEADY & WtLSON {1990) or SFORZA & BOURGOIN ( 1998) male and female during mating nre placed side by side, involving the twist of the male genital block. This copulatory position which must be maintained during the whole time of insemination is s trengthened by various morphological slJUCtures and not only by the male gonostyli.

Maintenance of the copulatory position is achieved slightly different.ly in the two Lophopidae examples studied here. In J ugoda the male gonostyli are inserted into the deep membranous intersegmenlal fold VII· Y111. With the pressure of tbe wide anal tube on the female abdomen they act as a clamp to maintllin in plaee the phallic complex. In Pyrilla the gonostyli are more reduced than those of Jugoda and only enclose each gonoplacs laterally while the anal tube. much more developed, hooks the seventh stemi1c. In both cases the aoal tube plays an irnponanr role 10 maintain the copulatory position. The role of the anal tube has already been expressed in various otlter Fulgoromorpha genera : in Cixius (WEDER, I 930) or in Hyalesthes (HOCH & REMANE, I 985 ; SFORZA & BOURGOIN, 1998) in Cixiidae, in Stenocranus in Delphacidae (ASCHE, 1985), in Colpop1era (MYERS, 1928) or in Hysre­roptenun (WEBER, 1930} in lssidae. However this is not a general pattern as such a role of the anal tube is absent in another Delphacidae genus, Prokelisia (HEADY & WILSON. 1990) and in the Tropiducbidae genus Trype1imorplra (BOURGOll'I & HUANG , 1991).

If we take into account : I) tliat modifications of the male anal tube shape are not necessary to assure the copulation ; 2) that widening or posterior development of the male anal tube is probably apornorphic, one ean raise the question of the adaptive value of the morphological modifications of the anal tube and if any selective pressure can be hypolhe· sised lo account these m~ifications

Deposit and storage of spermatozoa. - Different modes of sperm transfer, deposit and s torage within the female genitalia are known in Hemiptera. A particular mode is known in Stemorrhyncha Coccoidea where spennatozoa are transferred into !he female tractus via motile bundles of 16·64 or more spermato1.oa (ROBINSON, 1977). In some Auchenorrhyn· cha Cicadomorpha spermatozoa are not transferred free but connected to median rods for· ming spennatodesmes before being deposited into the bursa copulatrix (ROBERTSON & GIBBS, 1937; MAILLET, 1959; CHEVAILUER, 1962; Bout.ARD, 1965). This way ofspcnna· tozoa transfer is only known in Cercopidae (spem1atodesme of type I) or in Cicadidae, Ledri­dac and Ulopidae (spcrmatodesrne of type ll) while ii has never ~n observed in Membra­cidae, Cicadellidae and other Hemiptera.

Three modes of deposition and sperm storage are known within the Fulgoromorpba.

158 A. SOULIER-PERKINS & T. BOOROOIN

In the simplest one, spcnnatowa arc directly deposited into the spennathcca where they nrc stored (Tenigometridae T.uigomerra : BOURGOIN & HUANG , 1991 ). In the second mode, sperm is deposited free (probnbly with other male secretions) at the basis of dte bursa copu­lntrix or into it (Cixiidae, Hynlcsthcs : HOCH & RUMANU, 1985 ; SFORZA & BouROOtN, 1998. Delpbacidae, S1e11ocra111LS: Asche, 1985, and Tropiduchidae, Trypetimorpha: BOURGOIN & HUANG, 1991). Spcrmatowa have to migrate into the spermntheeu for storage. In the thin! mode. spermatozoa are first stored into a spermatophora produced by the male bef0<e being deposited within the female bursa copulatrix (Dyctyophuridae. Dycryophara : STROBL~G. 1955; Ocrbidac. Diostromb11s sp.: SFORZA & BOURGOIN. 1998). The spcnnarophore must be destr0yed lo release the speimatozoa which. after migration, will be then stored into the spcnnfatheca.

In the two Lophopidae genera studkd here the mllle gonoporus opens at the basis of the bursa copulatrix and of the entrance of die anterior vngina where the spenna101.oa are thus deposited, and not directly into the spermatheca where they have to migJ11te. We think tlml secretion Of the tegumentary glands of the bursa copulatrix might play OJI intponant role in the mobility of the spermatozoa and/or in the destruction of the spcrmalophore in excess as shown by 0 0\Jt..ARD in the Cicadidae (1965).

If diverse modes of spenn depositing are nOI o necessity to ensure the fecundation. what are the adopta1ive vtllues of these diverse behU\•ioors observed? ls a selective pressure implicaled to get such modifications ? ·

Copulatory m~hanlsm in Fulgoromorpha and sexual selection. - How cnn such different morphological and behavioural panems can be explained ? With respect 10 sexual selection, both femalcchoiee (intersexual selection) and male-male competition (intmsexual selection) can be ndvocnted, acting simultaneously or not (DARWIN, 1871 ). This field of research bas generated a lot of studies in insects (sec particularly TuoRNHILL & Al.COCK, 1983; BRAOBUl\Y & ANDERSSON, 1987). For EBERHARD (1985, 1990, 1991, 1994) female choice is probably the most important selective factor to explain the diversity of male geni­talia morphologies : females discriminare between males oo the basis of male genitalic Struc­tures, and males with favoured genitalic morphologies sire more offspring th~t others. However inter- or intrnsexual selection might favour male genitalic modifications (sperm displacement, clasping devices, special male adaptations •... ) that cin:umvcnt the females characteristics responsible for controlling fecundation (EBERHARD, 1985). In such cases. mon-cuts of female choice during copulation can result in emphasising a possible selective conirol by fcmllles in 1>re· or postcopulatory events leading to fertilisation (EBl!RHARD. 1985).

While m(1le·nHolc competition is considered 10 be of primary importance in plnn· 1hoppers and is well documented (reviewed in CL.ARIDGS & de VRrJER. 1994 ; Orr. 1994), no studies have auempted to detennine whether female choice occurs in this group. Orr ( 1994) concluded however that "the criteria for demonstrating female choice appear to have been met". According to this hypothesis. one can suppose that males of Fulgoromorpha should react to female choice and male-male competition pressures by short-cutting pan of the mating behaviour and placing their spcnn in a position that reduce the possibility of supplamation by the sperm of another male.

ln planthoppers where male cannot strongly hold the female because the anal tube is 100 shorr (despite the presence of the tenninal spine like nnal process), time rcqulrod for copulation migh1 be very shon : I second in Javcsclla pel/11cida (Delphacidae, CLAR.TIXill & de YRIJER, J 994), 3 seconds in Tagosodes (= Sogata) orizicoln (Delphacidae, Mc:MlwAN, 1963). Longer time has been recorded: 13-33 minutes in M11ellerianella (Dclphucidnc. vir· gin females, natural populations. DROSOPOuws. 1985). In most of these species, rejection behaviours by females have been observed : abdomen shaking, kicking males away, pro­jection of the ovipositor, ... (Boou. 1982: DROSOPOULOS, 1985 ; CLARIOOE tl al .. 1984: H!w>Y & DENNO, 1991 ). A str0nger clamping or hooking by the male for a longer time might

IS9

reJ>fCSClll one of these possible shor1·alls. It migh1 allow to avoid his rejection by the female (incersexualselection). to give time to the spermatozoa to migrate into the speonatheca whac they can be stored for fertilisation and limit the possibililies for other males to copula1e with the female (inttaScxual selection). 1be genera Pyril/a is a good candidate to illustrate these shorH:ut hypotheses. Indeed, in P. perpusilla (bearing as in P. protubera/Js a long hooking anal lube) lime for copulation exceeds 2h (KUMAAASlNOttU, 1996). In the Cixiidae/fya/.sthes a sirong clamping by the male has also been described and time required for copulation is 40 mm (HOCH & REMANE, J 985 ; SFORZA & BOUROOL'I, 1998).

A110~1cr lype of short-cul should be the direct spcm1 deposit inside the spcrmathccn as observed in Tettisometra sulphurea Mulsant & Rey (BOURGOIN & HUANG, 1991).

Testing the scenario. - Tcsis of these adoptntional hypotheses come under popula· 1ion s1udies - out of the scope of this smdy - which only cao tel.1 us if the function suppo· sed here for these morphological diversity is adaptive. However Eberhard's model supposes that ma.Jes mighl reacl 10 both inlcr· and intrasexual sclcc1ive pressures by generating shon­CUIS of the mating behaviour linked with m01phological modi6cations. Such models can be lested on the phylogeny (Eu>Rax;E & CRACRAPr, 1980 ; CARJ'EHTER, 1989 ; GRANDCOLAS et al., 1994. 1997: BOURGOL'I. 1997). Indeed if this scenario has some reality it mUSt cany some panem specificity {CODDINGTO)I, 1988, 1990) that can be used as a first cest of this hypolhesi.s. However, if the test is successful it will not give conclusive evidence that the explanation given here is correct (one does not test adapcation) but just that the scenario proposed is a possible explanation which is not falsified by the teSL

Subscqucmly, we have chooscn to tcsl if the hook·shnped or lateral and terminal wide· ning of the mule anal tube should be considered as having a role in short-cuting the female choice or male-male competition (fig. 15). Considering that these characters assume always

F'1.1. IS, chancier ·1111pe or 1be male a.naJ tube" oplimiscd on the LophopKI phylogeny areording to Soulier­PclJdru (1997).

the same function, they can be optimised on the phylogeny of the Lophopidae recently construc1cd by SOULIER-PERKINS (1997). These charac1ers have not been included in the matrix of the phylogeny but they have been plotcd on the cladogram. The most parsimoniou.s optimisation (5 steps) leds to conclude tha1 the hook-shaped and the lateral widened anal tubes are apomorpbic when the ancestor was bearing a simple shaped anal tube. If we fort:c the ancestor to present a long and hook-shaped anal tube, 6 steps are needed to explain the

160 A. SOULlllR-PlllUilllS & T. OOUROOIN

history oflhischaracter and 7 steps if lhc ancestor did posses an anal tube with lateral and ter­minal widening. The most parsimonioos optimisa1ion does DOI reject the bypolhcsis. The change in morphology for 1hc anal lube inlo un hook-shaped or lateral nnd npical widening, ror some 1axa, can be an adaplation or 1he males to an inlcrsexual and/or in1rasexual selcclion.

According to Coooi.'iOTON (1988) lhc hypolhesis can be supported if. I) lhc trail and iis function appear on lhe srunc node ; 2) the trait which supports the allcmative function (supposed Jess advamagcous) is plcsiomorphic. For now, not enough behavioural data arc cum:ntly known to assume llinl the uai.t and lhe function occulted in the same node. But such du tu could be cnsily checked in ru1ure behavioural studies. Those resulls focus on some new scientific perspectives to invcs1igFa1e.

CONCLUSION As in mos1 other insecl 1axa. slUdy or mating behaviour in planthoppcrs discloses a

greul diversi1y. Acoustic behuviours play surely a very imponnnt role (Ci.ARJDOe, 198~ : Cl.ARIDGE & de VRUER. 1994) bu1 they are very probably no1 lhc sole. copula1ory mecha­nisms needed to be lalren in consideration. 1l1cir diversity in plantboppers can be summa­rised as :

-copula1ion modes : monotrysian. ditrysian (BOURGOIN & HUANG, 1991) - sperm 1ransrer : directly or using a spcrmatophore - sperm deposit : ditcctly into the spennatbeca, at the bursa copulatrix ducrus level

or within the bursa - duralion or CogagemCOI : very short (fow seconds) 10 !WO hours (SO rar 31 it is cur­

rcnlJy known) - mllinlcnunce or copulmory position : l>y genitalic structures only. will11he belp of

pygofer processes and/or or lhc gonostyli and/or various devices us ing an:il morphologicul modifications.

The collection of more behavioural data is required if one should wish to investigate rurll1cr in order to organise lhis information with. regard 10 u belter underslanding of pla.11-lhopper evolu1ion. Currently. within the Lophopidae. the copulation limo, for the genus Pyrilla, is kuown and matches the morphology or the anal tube. Further studies should be done oo the copula1ion time Md specially ror 1hc genera presenting an anal 1ube with a late­ral and lerminal widening like Jugoda. The lest prese11led here and lhc heuristic power or the phylogeny could suggesl the suuting of lhis study wilh 1)1c genera Lapithasa and Clo­nospe.These genera occupy u basnl posi1ion in the two groups for which 1hc nnul tube is lulerally and apically widened.

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